DISEASE THREATS TO AMPHIBIAN POPULATIONS

Evan H Campbell Grant

Northeast Amphibian Research and Monitoring Initiative

US Geological Survey

Patuxent Wildlife Research Center

David E. Green, DVMUS Geological Survey

National Wildlife Health Center

David Miller

US Geological Survey

Patuxent Wildlife Research Center

Mitch Eaton

US Geological Survey

Patuxent Wildlife Research Center

Color slides of 5 common lethal infectious diseases of amphibians

Considerations for surveillance and monitoring of diseases at multiple scales

5 Common Lethal Infectious Diseases of Amphibians

- Chytrid Fungus- Ranaviruses- Perkinsus-like organism- Ichthyophonus sp.- Ribeiroia ondatrae (fluke)

1) Pathogenic Chytrid Fungus: Batrachochytrium dendrobatidis (“Bd”)

Major cause of amphibian population declines worldwide

Kills only frogs & toads after metamorphosis; occasionally lethal in adult newts

Die-offs are insidious; rarely are more than 2 dead frogs or toads found at a site

Mixed effect of disease on populations in northeastern US

Chytridiomycosis: Gross Findings: TadpolesLarvae: non-lethal oral infection of tadpoles

Chytridiomycosis: Gross Findings: Adult Frogs Lethal in majority of spp. within 2-3 wks of end of metamorphosis

Harlequin frog (Panama)Harlequin frog (Panama)

Chiricahua leopard frog (Rana chiricahuensis)

Bd: Salamanders

Pathogenicity largely unknown; non-lethal

to aquatic life-stages, occasionally

lethal to red-spotted newts.

Susceptibility of terrestrial salamanders is

largely unstudied

Stream salamanders susceptible; no die-offs

observed.

Chytridiomycosis in Amphibians Year of First Detection

Puerto Rico

c.’74c.’74

‘76‘76

c.’95c.’95

‘74‘74

‘00‘00

‘99‘99 ‘00‘00

‘99‘99

‘00‘00

‘77‘77

‘95‘95

‘00‘00

‘01‘01

‘02 ‘02

‘00‘00

‘01‘01

‘01‘01

‘97‘97

‘02‘02

‘02‘02

Revised Aug 2010

‘03 ‘03

‘01 ‘01

‘02 ‘02

‘04‘04

‘74‘74

‘03 ‘03

‘06 ‘06

Museum specimens

‘01 ‘01 ‘01 ‘01

2) Ranaviruses

Agent: Ranavirus; Family: Iridoviridae- 5 or 6 distinct strains or species in USA- Some strains are host-specific, other strains may be panzootic

Epizootiology:- Kills larvae & larvae in metamorphosis- Seldom affects adult amphibians in USA- Onset is sudden (explosive)- Mortality rate often >95% of larvae

Ranavirus Infection

Gross Findings:1. Petechia or ulcers in skin

Ranavirus InfectionGross Findings:2. Effusions under skin and into body cavity

Bunch of dead decaying tadpoles

Matt Gray, UT

Ranavirus Die-offs: Frogs and Toads (tadpoles)

Puerto Rico

Revised Aug 2010

Alaska

Hawai’i

Ranavirus Die-offs: Salamanders (larvae)

Puerto Rico

Revised Aug 2010

Alaska

Hawai’i

3) Perkinsus-like Organism • Kills ranid tadpoles only,

rarely other spp.

• Die-offs may continue for weeks with bloated weak tadpoles floating on surface

• Often causes >90% mortality of ranid tadpoles in a pond (hence, little recruitment)

Mississippi gopher frog (Rana sevosa)

- Mildly to massively enlarged light yellow liver, spleen, pronephroi & mesonephroi

- Abdominal distention

Perkinsus-like Organism: Gross Findings

Perkinsus-like Organism: Distribution

Puerto Rico

Revised Aug 2010

Alaska

Hawai’i

4) Ichthyophoniasis1. Definition: A slight to severe (and

lethal) infection of amphibian skeletal muscle

“Swollen rump” in recently metamorphosed frogs

Lethal Infections occur in

Eastern red-spotted newts Larval Rana spp.

Adult Rana spp.

Eastern red-spotted newt

Green frog

Amphibian Ichthyophoniasis: Distribution

Puerto Rico

Revised Aug 2010

Polymelia PolypodiaPolydactyly & Skin Web Ectromelia

Infection by metacercariae must occur at very specific tadpole ages to induce malformation (Gosner 26-28)

5) Ribeiroia ondatrae-induced Malformations:

Now that we know what we’re looking for…

And where it has been found…

Develop an efficient monitoring and surveillance program

Interest in diseases at multiple levelsMapping – detections/dieoffsNumber of ponds affectedPrevalence at an infected pondTemporal and spatial dynamicsPopulation-level effects

Two primary challenges

(1) addressing uncertainty with (only partially) observed disease dynamics in the wild

(2) determining how environmental, spatial, and community processes interact to cause outbreaks and disease persistence.

Challenge 1: Uncertainty (False positives and/or negatives)

McClintock et al. 2010. Ecol Lett. 13:659

Uncertainty at each level:Pr(Refuge contains disease)

Pr(Refuge contains disease)Pr(Pond diseased | Refuge diseased)

Pr(Refuge contains disease)Pr(Pond diseased | Refuge diseased)Pr(Frog diseased | Pond diseased)

Pr(Refuge contains disease)Pr(Pond diseased | Refuge diseased)Pr(Frog diseased | Pond diseased) Pr(Detect disease | Frog diseased)

Ignoring uncertainty

False + and/or – errorsResults in biased estimates of presence,

prevalence and dynamics.

We need to design methods and apply sampling to efficiently address these sources of uncertainty.Probabilistic choice of sampling unitsRepeat sampling in space and timeHow to allocate effort across the hierarchy?

2) Determining causes of outbreaks and disease persistence

Sampling design considerations (what, when, where)

Statistical methods which account for imperfect detection

Combinations of field and laboratory studies

Research needs:Pathogen ecologyReservoirs/vectors - persistenceMechanism(s) for outbreaksInfluence of spatial structure of habitats

Matt Gray, UT

Recommendations and challenges

Consider hierarchical nature of disease question (presence vs. prevalence; scale)?

Dynamics in presence and prevalence – annual allocation of effort

Uncertainty in ecology of many amphibian diseases.

Management? Working on developing amphibian disease

monitoring program for NE refuges - ehgrant@usgs.gov